Environmental Factors and Puberty Onset: An Update
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Journal of Biology and Life Science
ISSN 2157-6076
2014, Vol. 5, No. 2
Environmental Factors and Puberty Onset: An Update
Ghulam Nabi (Corresponding author)
M. Phil Scholar. Department: Animal sciences
Reproductive neuro-endocrinology Lab: Quaid-i-Azam University, (Islamabad) Pakistan
Tel: 92-345-811-2741 E-mail: ghulamnabiqau@gmail.com
Muhammad Amin
M. Phil Scholar, Department of Zoology, University of Karachi, Pakistan
Tel: 92-315-902-0833 E-mail: aminmuhammad013@yahoo.com
Rishma Sultan
M.Phil. Scholar, Department of Zoology
Islamia College University Peshawar, Khyber Pakhtunkhwa, Pakistan
E-mail: Mohdsaim94@gmail.com
Muhammad Kamil
M. Phil Scholar, Department of Botany, University of Malakand, Pakistan
Tel: 92-343-925-6626 E-mail: mohammadkamil86@gmail.com
Received: July 4, 2014 Accepted: July 20, 2014
doi:10.5296/jbls.v5i2.5911 URL: http://dx.doi.org/10.5296/jbls.v5i2.5911
Abstract
Puberty is a process that results from a coordinated series of complex neuroendocrine changes
which eventually leads to external and internal physical changes. These changes include
attainment of primary and secondary sexual characteristics. Puberty as a temporal process is
subdivided into different stages. These pubertal stages occur in a sequential manner but
significant variations have been seen among different individuals in the timings of pubertal
onset as well as a certain degree of gender difference is also present where puberty is occurring
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earlier in girls than boys. Among many aetiologies which have been hypothesized to be
involved, environmental cues are the most ones. This review article describes the recent
findings of the influences of the key environmental clues on pubertal timings, emphasizing on
the aspects for which the most scientific evidences exist.
Keywords: Puberty, Temporal, Neuroendocrine
1. Introduction
Sexual maturation in humans is physiological variation of pubertal age. Sexual maturation in
normal individuals dwelling in the same area is affected by genetics, ethnic, environmental and
nutritional factors (Gaudineau et al., 2010). Puberty onset is initiated by activation of
hypothalamic GnRH neurons which secrete pulses of gonadotropin-releasing hormone
(GnRH). This activation of GnRH pulses is also known as GnRH pulse generator activity and
stimulates the secretion of pituitary gonadotropic hormone downstream. Pituitary
gonadotropins acts on gonads and activate the process of steroid genesis and subsequent
maturation of gametes (Mayer et al., 2010). Average age of puberty onset has been declined
over the 20th and early 21st century especially in populations that are characterized by
improvements in socioeconomics or social conditions (Boynton-Jarrett and Harville, 2010).
Moreover, many studies showed marked differences in pubertal timing across different ethnic
groups. Varieties of genetic and environmental factors have been found to influence timing of
puberty. Environmental stressors and supports may accelerate or suppress the HPG axis by
influencing the biological stress responses to early adversities (Boynton-Jarrett and Harville,
2010). Environmental conditions that strongly influence the timing of puberty onset include (1)
photoperiod (2) nutrition (3) psychosocial factors and (4) endocrine disruptors (Deardroff et al.,
2011).
2. Psychosocial Factors
Exposure to a number of psychosocial stressors during pre-pubertal period such as (1)
immigration (2) neighborhood environment (3) father absence (4) socioeconomic status (5)
childhood social hardships and (6) food insecurity, alter the timing of puberty onset. Dramatic
changes in socio-economic context are also involved in altering the timings of puberty onset in
children (Tan and Camras, 2013).
2.1 Immigration
Immigration is reviewed as radical socio-cultural alteration for children. In immigration
nutritional upshot and quick weight growth following adoption may cause premature puberty
onset. Studies found the ubiquity of precocious puberty by the appearance of breast
development slightly earlier in adopted Chinese girls as compared to non-adopted American
girls (Tan and Camras, 2013).
2.2 Neighbourhood Environment
It also effect puberty onset by either “reduced physical activity or reduced access to healthful
foods” or through exposure to chronic and acute stressful familial environment. These factors
trigger puberty by influencing hormonal pathways. More recreational outlets in neighbourhood
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delayed timing of puberty onset in study area. Physical activity affects puberty timings by
influencing adiposity and body weight (Deardorff et al., 2012).
2.3 Father Absence and Socioeconomic Status
It influences pubertal initiation among adolescents. Recently, studies have associated early
onset of puberty to both lower household income and lower parental education. There is strong
association between early menarche and high socio-economic status among black girls and
vice versa in white girls. However parental education is not significant indicator of early
menarche (Braitchwaite et al., 2009). Another studies found that girls with absent biological
father from high SES exhibited precocious puberty than those having biological fathers in their
homes. In the case of low income families, there is no link between early menarche and father
absence (Deardroff et al., 2011; Belachew et al., 2011; James-Todd et al., 2010; Al-Sahab et al.,
2010). The possible cause of precocious puberty may possibly be the familial stress due to
maternal work load and diminution in maternal affection. Another reason might be the
acquaintance to high level of endocrine disrupters (i-e beauty products) or technology (video
games, internet) that increases disclosure to light and disturbs sleep-wake cycle which has been
linked to early menarche. Another study reveals the relationship between early puberty onset
and single parenting as a psychosocial among Mexican-American girls (Jean et al., 2010).
2.4 Childhood Social Hardships
These also play critical role in pubertal timings. (1)Stressful home circumstances (2) family
conflicts (3) alterations in family structure (4) attachment relationships (5) child maltreatment
(6) parental divorce (7) low parental involvement and (8) marital conflict , all lead to early
menarche and precocious sexual maturation through chronic elevation of HPG and HPA
axis.(Jean et al., 2010; Boynton-Jarrett et al.,2010) Physical abuse is weakly associated with
early menarche while sexual abuse has strong association (Boynton-Jarrett et al., 2010).
Overwhelmingly, we can say that children exposed to cumulative aversive condition would
have altered timings of puberty. Vigorous physical activity is accompanying with decreased
estrogen secretion and increased age at menarche due to disturbance of GnRH pulsatility
(Belachew et al., 2011).
2.5 Food Insecurity
Studies found that stress and anxiety about food availability or insufficient access to energy,
delays menarche by one year. Malnutrition and increased energy expenditure are also linked
with delayed menarche. Age at menarche has declined over last two centuries in most part of
the world due to improvement in nutrition and population health (Belachew et al., 2011).
Early family environment covaries with menarcheal age as a function of polymorphic variation
in estrogen receptor-α (ESR1)
Studies reported in European-American women that girls reach to puberty at later age that
belongs from healthy environment and cohesive families and in contrary those girls who
belong from conflicted or divorced families reach to early menarche. This link is regulated by
polymorphic variation in the gene encoding estrogen receptor-α (ESR1). Moreover correlated
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variations of family environment positively regulated menarcheal age in those applicants
homozygous for minor alleles (rs9304799, rs2234693), but not in women having different
genotypes (Manuck et al., 2011). These findings are consistent with hypothesis of Belsky and
Pluess, 2009 who found that girls differ genetically in their sensitivity to rearing effects on
pubertal maturation.
3. Endocrine Disruptors and Puberty
Recent studies have demonstrated a progressive decrease in age of onset of puberty in children
around the world. Perhaps, it is due to complex interaction between genetics, endocrine and
environmental factors. The process of industrialization results into a gradual, but significant
increase in number and amount of environmental pollutants. Some of these environmental
pollutants are natural or synthetic chemicals with alarming effects on the endocrine system.
The chemicals that affect the endocrine system are called endocrine disruptors (EDs). Various
epidemiological studies on exposure of EDCs show variable tendency towards the puberty
onset. In this regard, some EDCs advance puberty, some delay puberty, while others show no
association.
To estimate the potential of EDCs which advances the puberty onset, following studies are
noteworthy. Prepubertal administration of bisphenol A (BPA) at different doses significantly
decreased the body weight from (PND) post natal day 18 to 30. Moreover, bisphenol advances
the puberty timing significantly in treated group as compared to control group. BPA induce this
effect through its estrogenic activity (Won et al., 2011). In cohort study, exposure of
diethylstilbestrol (DES) during the first 15+ week in both lowJournal of Biology and Life Science
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2014, Vol. 5, No. 2
(Jawahar et al., 2011). Similarly, the effect of blood lead levels on puberty onset demonstrated
in cohort study of African population in which blood sample were taken to analyze the lead
level from 712 girls who had the menarche data. This study found that lead even at low dose (5
μg/dl) blood levels may delay the onset of puberty among adolescent girls. While, higher blood
lead levels were associated with significant delays in the onset of puberty (pJournal of Biology and Life Science
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2014, Vol. 5, No. 2
intake may experience their onset of breast development and reach their peak height velocity
approximately 7–8 months later than girls with the lowest levels of intake (Guo et al., 2012).
The adipose derived hormone leptin and gastrointestinal-derived hormone ghrelin
communicate information about metabolic status and body weight to the hypothalamus to
initiate puberty, so ghrelin and leptin represent metabolic gate for puberty (El-Eshmawy et al.,
2010).
Secular trends toward a declining age at puberty onset with correlated changes in body weight
have been reported in economically advanced countries. This has been attributed to excess
calorie intake along with reduced physical activity in children. However, because the timing of
puberty in humans is also influenced by other factors, such as genetic traits, living conditions,
geographical location, and environmental chemicals, it is difficult to distinguish the effect of
diet and body size from other factors in a human population. Feeding juvenile female Rhesus
monkeys with a high-calorie diet results in acceleration of body growth and precocious
menarche, the monkeys fed a high calorie diet also had an elevated body mass index (Teraswa
et al., 2012). From the above experiment we concluded that nutrition have great impact on the
onset of puberty, those individuals which have healthy diet in their juvenile period have reach
puberty earlier than those which have poor calories diet or malnutrition .
5. Photoperiod
In case of seasonal breeders, photoperiodic cues have a strong influence on the onset of puberty
and first reproduction, helping the animals to adjust their breeding seasons to the most
appropriate season. Pregnant females transfer information about photoperiod to developing
fetus via blood through melatonin. Females born into decreasing photoperiods delayed
maturation by about 30 days (Fritz et al., 2010). In fish, in vivo hypothalamic sGnRH,
cGnRH-II, Kiss-1 receptor, pituitary GTHα mRNA, LH-β2 and FSH-β mRNA, Kiss 1 mRNA
17α-hydroxypregnenolone and LH level increases when exposed to green LED for 4 month.
Culture cell exposed to green LED only and red LED only shows that green LED significantly
increases hypothalamic sGnRH, cGnRH-II, Kiss-1 receptor, Kiss 1 mRNA, GTHα mRNA,
LH-β2 and FSH-β level, but no significant change were observed for red LED exposure except
GTHα and LH-β2 mRNA level (Hyun et al., 2013). Greater the exposure time to light, early
will be the onset of puberty. Studies found that when female Japanese quails were transferred
from short days to long days causes significant increase in LH, FSH, 17β-oestradiol and ovary
weights while T3, Progesterone and prolactin level decreases but no significant changes were
observed in T4 concentrations. The results were opposite when female quails were transferred
from long days to short days, still the T4 level was not significantly changed (Henare et al.,
2012). According to another studies, photoperiodic changes in kisspeptin level is due to
changes in photoperiod driven by the changes in the pattern of melatonin secretion, suggesting
melatonin receptor on kisspeptin neurons. This causes increase cellular expression (Kiss1
mRNA and kisspeptin protein) and number of kisspeptin terminal appositions to GnRH
neurons (Smith and Clark, 2010). Another similar study, stated that pinealectomy and/or
replacement of physiological concentrations and patterns of melatonin in sheep, rhesus
monkeys and various hamster species provide convincing evidence that melatonin really is the
key hormone regulating the seasonal timing of puberty (Ebling, 2010).
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6. Conclusion
In summary, many studies and evidences suggest that environmental cues play a central role in
controlling the timing of pubertal onset through activation of GnRH– gonadotropin axis. These
factors range from nutrition and social stress to wide range of endocrine disruptors in our
environment. So, it cannot be concluded that any factor, alone alters the timing of puberty
onset.
Altered puberty timing causes serious health concerns. Early pubertal onset contributes to both
short-term and longer-term negative health outcomes including obesity, reproductive cancers,
and cardiovascular disease. Women with early menarche are more susceptible to engross in
early sexual activities, smoking, alcohol abuse and maternal conflictions. Further studies are
needed to address all the environmental cues that affect the puberty onset and best ways to
eliminate exposure to them, in order to improve health conditions in our future generations.
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